Pubertal bisphenol A exposure alters murine mammary stem cell function leading to early neoplasia in regenerated glands

Cancer Prevention Research

Volumn 7, Issue 4, 2014, Pages 445-455

  Wang, Danhan ^a,b   Gao, Hui ^a,b   Bandyopadhyay, Abhik ^b,c   Wu, Anqi ^a,b   Yeh, I Tien ^d   Chen, Yidong ^c   Zou, Yi ^c   Huang, Changjiang ^a   Walter, Christi A ^b,c   Dong, Qiaoxiang ^a,b   Sun, Lu Zhe ^b,c  

^a WENZHOU MEDICAL UNIVERSITY   (China)

^b Mays Cancer Center at UT Health San Antonio   (United States)

^c UNIVERSITY OF TEXAS HEALTH SCIENCE CENTER AT SAN ANTONIO   (United States)

^d VIRGINIA HOSPITAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

4,4' ISOPROPYLIDENEDIPHENOL; 7,12 DIMETHYLBENZ[A]ANTHRACENE; BENZHYDRYL DERIVATIVE; MESSENGER RNA; PHENOL DERIVATIVE; SCAVENGER; TUMOR MARKER;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BRANCHING MORPHOGENESIS; BREAST CARCINOGENESIS; BREAST CELL; BREAST HYPERPLASIA; BREAST TUMOR; CANCER SUSCEPTIBILITY; CELL FUNCTION; CELL ISOLATION; CONTROLLED STUDY; EARLY CANCER; EXPOSURE; FEMALE; GENE EXPRESSION; GROUPS BY AGE; MALIGNANT TRANSFORMATION; MAMMARY GLAND; MOUSE; NONHUMAN; PERINATAL PERIOD; PRIORITY JOURNAL; PUBERTY; RNA SEQUENCE; SEQUENCE ANALYSIS; STEM CELL; ANIMAL; BAGG ALBINO MOUSE; CELL CULTURE; CELL PROLIFERATION; CELL TRANSFORMATION; CHEMICALLY INDUCED; DNA MICROARRAY; DRUG EFFECTS; EXPERIMENTAL MAMMARY NEOPLASM; FLOW CYTOMETRY; GENE EXPRESSION PROFILING; GENETICS; HUMAN; METABOLISM; NUDE MOUSE; PATHOLOGY; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TOXICITY; UDDER;

ANIMALS; BENZHYDRYL COMPOUNDS; CELL PROLIFERATION; CELL TRANSFORMATION, NEOPLASTIC; CELLS, CULTURED; FEMALE; FLOW CYTOMETRY; FREE RADICAL SCAVENGERS; GENE EXPRESSION PROFILING; HUMANS; MAMMARY GLANDS, ANIMAL; MAMMARY NEOPLASMS, ANIMAL; MICE; MICE, INBRED BALB C; MICE, NUDE; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PHENOLS; REAL-TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; STEM CELLS; TUMOR MARKERS, BIOLOGICAL;

EID: 84898918955     PISSN: 19406207     EISSN: 19406215     Source Type: Journal    
DOI: 10.1158/1940-6207.CAPR-13-0260     Document Type: Article

References (46)

1. Vandenberg LN, Maf fini MV, Wadia PR, Sonnenschein C, Rubin BS, Soto AM. Exposure to environmentally relevant doses of the xenoestrogen bisphenol-A alters development of the fetal mouse mammary gland. Endocrinology 2007;148:116-27. (Pubitemid 46021444)
2. Prins GS, Tang WY, Belmonte J, Ho SM. Developmental exposure to bisphenol A increases prostate cancer susceptibility in adult rats: epigenetic mode of action is implicated. Fertil Steril 2008;89:e41. (Pubitemid 351749388)
3. Soto AM, Vandenberg LN, Maffini MV, Sonnenschein C. Does breast cancer start in the womb? Basic Clin Pharmacol 2008;102:125-33. (Pubitemid 351143422)
4. Markey CM, Luque EH, de Toro MM, Sonnenschein C, Soto AM. In utero exposure to bisphenol A alters the development and tissue organization of the mouse mammary gland. Biol Reprod 2001;65:1215-23. (Pubitemid 32927590)
5. Nikaido Y, Yoshizawa K, Danbara N, Tsujita-Kyutoku M, Yuri T, Uehara N, et al. Effects of maternal xenoestrogen exposure on development of the reproductive tract and mammary gland in female CD-1 mouse offspring. Reprod Toxicol 2004;18:803-11. (Pubitemid 38987967)
6. Munoz-de-Toro M, Markey CM, Wadia PR, Luque EH, Rubin BS, Sonnenschein C, et al. Perinatal exposure to bisphenol-A alters peri-pubertal mammary gland development in mice. Endocrinology 2005;146:4138-47. (Pubitemid 41175786)
7. Ayyanan A, Laribi O, Schuepbach-Mallepell S, Schrick C, Gutierrez M, Tanos T, et al. Perinatal exposure to bisphenol A increases adult mammary gland progesterone response and cell number. Mol Endocrinol 2011;25:1915-23.
8. Durando M, Kass L, Piva J, Sonnenschein C, Soto AM, Luque EH, et al. Prenatal bisphenol A exposure induces preneoplastic lesions in the mammary gland in Wistar rats. Environ Health Persp 2007;115:80-6. (Pubitemid 46050286)
9. Murray TJ, Maffini MV, Ucci AA, Sonnenschein C, Soto AM. Induction of mammary gland ductal hyperplasias and carcinoma in situ following fetal bisphenol A exposure. Reprod Toxicol 2007;23:383-90. (Pubitemid 46602926)
10. Jenkins S, Raghuraman N, Eltoum I, Carpenter M, Russo J, Lamartiniere CA. Oral exposure to bisphenol a increases dimethylbenzan-thracene- induced mammary cancer in rats. Environ Health Persp 2009;117:910-5.
11. Betancourt AM, Eltoum IA, Desmond RA, Russo J, Lamartiniere CA. In utero exposure to bisphenol a shifts the window of susceptibility for mammary carcinogenesis in the rat. Environ Health Persp 2010;118: 1614-9.
12. Tharp AP, Maffini MV, Hunt PA, VandeVoort CA, Sonnenschein C, Soto AM. Bisphenol A alters the development of the rhesus monkey mammary gland. Proc Natl Acad Sci U S A 2012;109:8190-5.
13. Yang L, Luo L, Ji W, Gong C, Wu D, Huang H, et al. Effect of low dose bisphenol A on the early differentiation of human embryonic stem cells into mammary epithelial cells. Toxicol Lett 2013;218:187-93.
14. Fenton SE, Reed C, Newbold RR. Perinatal environmental exposures affect mammary development, function, and cancer risk in adulthood. Annu Rev Pharmacol 2012;52:455-79.
15. Shackleton M, Vaillant F, Simpson KJ, Stingl J, Smyth GK, Asselin- Labat ML, et al. Generation of a functional mammary gland from a single stem cell. Nature 2006;439:84-8. (Pubitemid 43053633)
16. Stingl J, Eirew P, Ricketson I, Shackleton M, Vaillant F, Choi D, et al. Purification and unique properties of mammary epithelial stem cells. Nature 2006;439:993-7. (Pubitemid 43292419)
17. Spike BT, Engle DD, Lin JC, Cheung SK, La J, Wahl GM. A mammary stem cell population identified and characterized in late embryogenesis reveals similarities to human breast cancer. Cell Stem Cell 2012;10:183-97.
18. Cicalese A, Bonizzi G, Pasi CE, Faretta M, Ronzoni S, Giulini B, et al. The tumor suppressor p53 regulates polarity of self-renewing divisions in mammary stem cells. Cell 2009;138:1083-95.
19. Lim E, Vaillant F, Wu D, Forrest NC, Pal B, Hart AH, et al. Aberrant luminal progenitors as the candidate target population for basal tumor development in BRCA1 mutation carriers. Nat Med 2009;15:907-13.
20. Shimono Y, Zabala M, Cho RW, Lobo N, Dalerba P, Qian DL, et al. Downregulation of miRNA-200c links breast cancer stem cells with normal stem cells. Cell 2009;138:592-603.
21. Molyneux G, Geyer FC, Magnay FA, McCarthy A, Kendrick H, Natrajan R, et al. BRCA1 basal-like breast cancers originate from luminal epithelial progenitors and not from basal stem cells. Cell Stem Cell 2010;7:403-17.
22. Prat A, Parker JS, Karginova O, Fan C, Livasy C, Herschkowitz JI, et al. Phenotypic and molecular characterization of the claudin-low intrinsic subtype of breast cancer. Breast Cancer Res 2010;12:R68.
23. Jenkins S, Wang J, Eltoum I, Desmond R, Lamartiniere CA. Chronic oral exposure to bisphenol a results in a nonmonotonic dose-response in mammary carcinogenesis and metastasis in MMTV-erbB2 mice. Environ Health Persp 2011;119:1604-9.
24. Jones LP, Sampson A, Kang HJ, Kim HJ, Yi YW, Kwon SY, et al. Loss of BRCA1 leads to an increased sensitivity to bisphenol A. Toxicol Lett 2010;199:261-8.
25. Vandenberg LN, Colborn T, Hayes TB, Heindel JJ, Jacobs DR, Lee DH, et al. Hormones and endocrine-disrupting chemicals: low-dose effects and nonmonotonic dose-responses. Endocr Rev 2012;33: 378-455.
26. Taylor JA, vom Saal FS, Welshons WV, Drury B, Rottinghaus G, Hunt PA, et al. Similarity of bisphenol a pharmacokinetics in rhesus monkeys and mice: relevance for human exposure. Environ Health Persp 2011;119:422-30.
27. Vandenberg LN, Chahoud I, Heindel JJ, Padmanabhan V, Paumgartten FJR, Schoenfelder G. Urinary, circulating, and tissue biomonitoring studies indicate widespread exposure to bisphenol A. Environ Health Persp 2010;118:1055-70.
28. Bandyopadhyay A, Dong Q, Sun LZ. Stem/progenitor cells in murine mammary gland: isolation and functional characterization. Methods Mol Biol 2012;879:179-93.
29. Dong Q, Wang D, Bandyopadhyay A, Gao H, Moncada K, Hildreth K, et al. Mammospheres from murine mammary stem cell-enriched basal cells: clonal characteristics and repopulating potential. Stem Cell Res 2013;10:396-404.
30. Stingl J. Detection and analysis of mammary gland stem cells. J Pathol 2009;217:229-41.
31. Medina D. The mammary gland: a unique organ for the study of development and tumorigenesis. J Mammary Gland Biol 1996;1:5-19.
32. Nelson JF, Felicio LS, Randall PK, Sims C, Finch CE. A longitudinal-study of estrous cyclicity in aging C57bl-6j mice: 1. cycle frequency, length and vaginal cytology. Biol Reprod 1982;27:327-39. (Pubitemid 13230807)
33. Langmead B, Trapnell C, Pop M, Salzberg SL. Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol 2009;10:R25.
34. HTseq. Available from: http://www.huber.embl.de/users/anders/HTSeq/.
35. Anders S, Huber W. Differential expression analysis for sequence count data. Genome Biol 2010;11:R106.
36. Benjamini Y, Hochberg Y. Controlling the false discovery rate-a practical and powerful approach to multiple testing. J Roy Stat Soc B Met 1995;57:289-300.
37. R/heatmap2. Available from: http://www.r-project.org/.
38. Database for annotation, visualization and integrated discovery (DAVID). Available from: http://david.abcc.ncifcrf.gov/.
39. Joshi PA, Jackson HW, Beristain AG, Di Grappa MA, Mote PA, Clarke CL, et al. Progesterone induces adult mammary stem cell expansion. Nature 2010;465:803-7.
40. Tripathi A, King C, De la Morenas A, Perry VK, Burke B, Antoine GA, et al. Gene expression abnormalities in histologically normal breast epithelium of breast cancer patients. Int J Cancer 2008;122: 1557-66. (Pubitemid 351294964)
41. Lindeman GJ, Visvader JE. Cell fate takes a slug in BRCA1-associated breast cancer. Breast Cancer Res 2011;13:306.
42. Asselin-Labat ML, Vaillant F, Sheridan JM, Pal B, Wu D, Simpson ER, et al. Control of mammary stem cell function by steroid hormone signalling. Nature 2010;465:798-802.
43. Haslam SZ, Bern HA. Histopathogenesis of 7,12-diemthylbenz(a) anthracene-induced rat mammary tumors. Proc Natl Acad Sci U S A 1977;74:4020-4. (Pubitemid 8197766)
44. Shen Q, Brown PH. Novel agents for the prevention of breast cancer: targeting transcription factors and signal transduction pathways. J Mammary Gland Biol Neoplasia 2003;8:45-73. (Pubitemid 38129950)
45. Lemmen JG, Broekhof JL, Kuiper GG, Gustafsson JA, van der Saag PT, van der Burg B. Expression of estrogen receptor alpha and beta during mouse embryogenesis. Mech Dev 1999;81:163-7. (Pubitemid 29183054)
46. Van Keymeulen A, Rocha AS, Ousset M, Beck B, Bouvencourt G, Rock J, et al. Distinct stem cells contribute to mammary gland development and maintenance. Nature 2011;479:189-U58.